SUMO and cellular adaptive mechanisms

다국어 초록 (Multilingual Abstract)

The ubiquitin family member SUMO is a covalent regulator of proteins that functions in response to various stresses, and defects in SUMO-protein conjugation or deconjugation have been implicated in multiple diseases. The loss of the Ulp2 SUMO protease, which reverses SUMO-protein modifications, in the model eukaryote Saccharomyces cerevisiae is severely detrimental to cell fitness and has emerged as a useful model for studying how cells adapt to SUMO system dysfunction. Both short-term and long-term adaptive mechanisms are triggered depending on the length of time cells spend without this SUMO chain-cleaving enzyme. Such short-term adaptations include a highly specific multichromosome aneuploidy and large changes in ribosomal gene transcription. While aneuploid ulp2Δ cells survive, they suffer severe defects in growth and stress resistance. Over many generations, euploidy is restored, transcriptional programs are adjusted, and specific genetic changes that compensate for the loss of the SUMO protease are observed. These long-term adapted cells grow at normal rates with no detectable defects in stress resistance. In this review, we examine the connections between SUMO and cellular adaptive mechanisms more broadly

참고문헌 (Reference)

1 Mulla, W., "Yeast : a simple model system to study complex phenomena of aneuploidy" 38 : 201-212, 2014

2 Westergard, L., "Wild yeast harbour a variety of distinct amyloid structures with strong prion-inducing capabilities" 92 : 183-193, 2014

3 Fischer, U., "Tumor hypoxia : Impact on gene amplification in glioblastoma" 33 : 509-515, 2008

4 Zhang, Z., "Transposon-mediated adaptive and directed mutations and their potential evolutionary benefits" 21 : 59-70, 2011

5 Pybus C., "Transcription-associated mutation in Bacillus subtilis cells under stress" 192 : 3321-3328, 2010

6 Shor, E., "The yeast environmental stress response regulates mutagenesis induced by proteotoxic stress" 9 : e1003680-, 2013

7 Li, S. J., "The yeast ULP2(SMT4)gene encodes a novel protease specific for the ubiquitin-like Smt3 protein" 20 : 2367-2377, 2000

8 Baldwin, M. L., "The yeast SUMO isopeptidase Smt4/Ulp2 and the polo kinase Cdc5 act in an opposing fashion to regulate sumoylation in mitosis and cohesion at centromeres" 8 : 3406-3419, 2009

9 Hetz, C., "The unfolded protein response and cell fate control" 69 : 169-181, 2018

10 Sheltzer, J. M., "The aneuploidy paradox: costs and benefits of an incorrect karyotype" 27 : 446-453, 2011

11 Ryu H. Y., "The Ulp2 SUMO protease promotes transcription elongation through regulation of histone sumoylation" 38 : e102003-, 2019

12 Lewicki, M. C., "The S. cerevisiae SUMO stress response is a conjugation-deconjugation cycle that targets the transcription machinery" 118 : 39-48, 2015

13 Chymkowitch P., "Sumoylation of Rap1 mediates the recruitment of TFIID to promote transcription of ribosomal protein genes" 25 : 897-906, 2015

14 Flotho, A., "Sumoylation : a regulatory protein modification in health and disease" 82 : 357-385, 2013

15 Enserink J. M., "Sumo and the cellular stress response" 10 : 4-, 2015

16 Sramko, M., "Stress-induced inactivation of the c-Myb transcription factor through conjugation of SUMO-2/3 proteins" 281 : 40065-40075, 2006

17 Cipponi, A., "Stress-induced cellular adaptive strategies : ancient evolutionarily conserved programs as new anticancer therapeutic targets" 36 : 552-560, 2014

18 Comerford K. M., "Small ubiquitin-related modifier-1 modification mediates resolution of CREB-dependent responses to hypoxia" 100 : 986-991, 2003

19 Huang, T. T., "Sequential modification of NEMO/IKKgamma by SUMO-1 and ubiquitin mediates NFkappaB activation by genotoxic stress" 115 : 565-576, 2003

20 Nguyen, A., "Selective Inbreeding: genetic crosses drive apparent adaptive mutation in the Cairnsfoster system of Escherichia coli" 214 : 333-354, 2020

21 Tempe, D., "SUMO under stress" 36 : 874-878, 2008

22 Finkbeiner, E., "SUMO routes ribosome maturation" 2 : 527-532, 2011

23 Seeler, J. S., "SUMO and the robustness of cancer" 17 : 184-197, 2017

24 Magwene P. M., "Revisiting Mortimer’s genome renewal hypothesis: heterozygosity, homothallism, and the potential for adaptation in yeast" 781 : 37-48, 2014

25 Hong Y., "Regulation of heat shock transcription factor 1 by stress-induced SUMO-1 modification" 276 : 40263-40267, 2001

26 Bossis, G., "Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes" 21 : 349-357, 2006

27 Bindra, R. S., "Regulation of DNA repair in hypoxic cancer cells" 26 : 249-260, 2007

28 Galluzzi, L., "Regulated cell death and adaptive stress responses" 73 : 2405-2410, 2016

29 Trachootham, D., "Redox regulation of cell survival" 10 : 1343-1374, 2008

30 Johnson E. S., "Protein modification by SUMO" 73 : 355-382, 2004

31 Yang Y., "Protein SUMOylation modification and its associations with disease" 7 : 2017

32 Hara, T., "Possible role of adaptive mutation in resistance to antiandrogen in prostate cancer cells" 65 : 268-275, 2005

33 Selmecki A. M., "Polyploidy can drive rapid adaptation in yeast" 519 : 349-352, 2015

34 Mo, Y. Y., "Overexpression of a dominant-negative mutant Ubc9 is associated with increased sensitivity to anticancer drugs" 64 : 2793-2798, 2004

35 Mo, Y. Y., "Nucleolar delocalization of human topoisomerase I in response to topotecan correlates with sumoylation of the protein" 277 : 2958-2964, 2002

36 Heidenreich, E., "Non-homologous end joining as an important mutagenic process in cell cycle-arrested cells" 22 : 2274-2283, 2003

37 Chu L., "Multiple myeloma-associated chromosomal translocation activates orphan snoRNA ACA11 to suppress oxidative stress" 122 : 2793-2806, 2012

38 Xu Z., "Molecular basis of the redox regulation of SUMO proteases : a protective mechanism of intermolecular disulfide linkage against irreversible sulfhydryl oxidation" 22 : 127-137, 2008

39 Harris R. S., "Mismatch repair protein MutL becomes limiting during stationary-phase mutation" 11 : 2426-2437, 1997

40 Levine, R. L., "Methionine residues as endogenous antioxidants in proteins" 93 : 15036-15040, 1996

41 Luo, S., "Methionine in proteins defends against oxidative stress" 23 : 464-472, 2009

42 Foster P. L., "Mechanisms of stationary phase mutation: a decade of adaptive mutation" 33 : 57-88, 1999

43 Yewdell, J. W., "Making sense of mass destruction: quantitating MHC class I antigen presentation" 3 : 952-961, 2003

44 Ryu, H. Y., "Loss of the SUMO protease Ulp2 triggers a specific multichromosome aneuploidy" 30 : 1881-1894, 2016

45 Giorgi, G., "LINE-1 retrotransposition in human neuroblastoma cells is affected by oxidative stress" 346 : 383-391, 2011

46 Reimers, J. M., "Increased transcription rates correlate with increased reversion rates in leuB and argH Escherichia coli auxotrophs" 150 : 1457-1466, 2004

47 Shao R., "Increase of SUMO-1 expression in response to hypoxia : direct interaction with HIF-1alpha in adult mouse brain and heart in vivo" 569 : 293-300, 2004

48 Raghavan V., "Incompatibilities in mismatch repair genes MLH1-PMS1contribute to a wide range of mutation rates in human isolates of Baker’s yeast" 210 : 1253-1266, 2018

49 Nathan D., "Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications" 20 : 966-976, 2006

50 Fabrizio, P., "Histone methylation and memory of environmental stress" 8 : 2019

51 Kregel K. C., "Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance" 92 : 2177-2186, 2002

52 Nefkens I., "Heat shock and Cd2+ exposure regulate PML and Daxx release from ND10 by independent mechanisms that modify the induction of heat-shock proteins 70 and 25 differently" 116 : 513-524, 2003

53 Peter J., "Genome evolution across 1, 011 Saccharomyces cerevisiae isolates" 556 : 339-344, 2018

54 Saitoh, H., "Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3" 275 : 6252-6258, 2000

55 Hickey, C. M., "Function and regulation of SUMO proteases" 13 : 755-766, 2012

56 Panse V. G., "Formation and nuclear export of preribosomes are functionally linked to the small-ubiquitin-related modifier pathway" 7 : 1311-1321, 2006

57 Zaher, H. S., "Fidelity at the molecular level: lessons from protein synthesis" 136 : 746-762, 2009

58 Rosenberg S. M., "Evolving responsively: adaptive mutation" 2 : 504-515, 2001

59 Haag K. L., "Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites" 111 : 15480-15485, 2014

60 Hochstrasser M., "Evolution and function of ubiquitin-like protein-conjugation systems" 2 : E153-E157, 2000

61 Bucher, E., "Epigenetic control of transposon transcription and mobility in Arabidopsis" 15 : 503-510, 2012

62 Pavelka, N., "Dr Jekyll and Mr Hyde: role of aneuploidy in cellular adaptation and cancer" 22 : 809-815, 2010

63 Bossis G., "Down-regulation of c-Fos/c-Jun AP-1 dimer activity by sumoylation" 25 : 6964-6979, 2005

64 Weaver, B. A., "Does aneuploidy cause cancer?" 18 : 658-667, 2006

65 Ryu H. Y., "Distinct adaptive mechanisms drive recovery from aneuploidy caused by loss of the Ulp2 SUMO protease" 9 : 5417-, 2018

66 Nguea, P. A., "Desumoylation of RNA polymerase III lies at the core of the Sumo stress response in yeast" 294 : 18784-18795, 2019

67 Jacquiau H. R., "Defects in SUMO(small ubiquitin-related modifier)conjugation and deconjugation alter cell sensitivity to DNA topoisomerase Iinduced DNA damage" 280 : 23566-23575, 2005

68 Mihaylova V. T., "Decreased expression of the DNA mismatch repair gene Mlh1 under hypoxic stress in mammalian cells" 23 : 3265-3273, 2003

69 Munoz-Lopez, M., "DNA transposons : nature and applications in genomics" 11 : 115-128, 2010

70 Roos, W. P., "DNA damage-induced cell death by apoptosis" 12 : 440-450, 2006

71 Huang, W. C., "Crystal structures of the human SUMO-2 protein at 1.6 A and 1.2 A resolution: implication on the functional differences of SUMO proteins" 271 : 4114-4122, 2004

72 Yona A. H., "Chromosomal duplication is a transient evolutionary solution to stress" 109 : 21010-21015, 2012

73 Fernandez, C., "Cholesterol is essential for mitosis progression and its deficiency induces polyploid cell formation" 300 : 109-120, 2004

74 Dunham M. J., "Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae" 99 : 16144-16149, 2002

75 Fulda, S., "Cellular stress responses: cell survival and cell death" 2010 : 214074-, 2010

76 Gordon, D. J., "Causes and consequences of aneuploidy in cancer" 13 : 189-203, 2012

77 Miranda I., "Candida albicans CUG mistranslation is a mechanism to create cell surface variation" 4 : 2013

78 Raghavan, V., "Baker’s yeast clinical isolates provide a model for how pathogenic yeasts adapt to stress" 35 : 804-817, 2019

79 Datta, A., "Association of increased spontaneous mutation rates with high levels of transcription in yeast" 268 : 1616-1619, 1995

80 Sheltzer J. M., "Aneuploidy drives genomic instability in yeast" 333 : 1026-1030, 2011

81 Kwon-Chung, K. J., "Aneuploidy and drug resistance in pathogenic fungi" 8 : e1003022-, 2012

82 Pan T., "Adaptive translation as a mechanism of stress response and adaptation" 47 : 121-137, 2013

83 Foster P. L., "Adaptive mutation: implications for evolution" 22 : 1067-1074, 2000

84 Heidenreich E., "Adaptive mutation in Saccharomyces cerevisiae" 42 : 285-311, 2007

85 Weil T., "Adaptive mistranslation accelerates the evolution of fluconazole resistance and induces major genomic and gene expression alterations in Candida albicans" 2 : 2017

86 Ryu, H. Y., "Adaptive aneuploidy counters a dysregulated SUMO system" 16 : 383-385, 2017

87 Hastings, P. J., "Adaptive amplification : an inducible chromosomal instability mechanism" 103 : 723-731, 2000

88 Ponder, R. G., "A switch from high-fidelity to error-prone DNA double-strand break repair underlies stress-induced mutation" 19 : 791-804, 2005

89 Kim S. K., "A model of liver carcinogenesis originating from hepatic progenitor cells with accumulation of genetic alterations" 134 : 1067-1076, 2014

90 Hendriks, I. A., "A comprehensive compilation of SUMO proteomics" 17 : 581-595, 2016